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Differential Occupation of Axial Morphospace

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Differential Occupation of Axial Morphospace Zoology 117 (2014) 70–76 Contents lists available at ScienceDirect Zoology jou rnal homepage: www.elsevier.com/locate/zool ଝ Differential occupation of axial morphospace a,∗ b Andrea B. Ward , Rita S. Mehta a Department of Biology, Adelphi University, 1 South Avenue, Garden City, NY 11530, USA b Long Marine Lab, Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA a r t a b i s c l e i n f o t r a c t Article history: The postcranial system is composed of the axial and appendicular skeletons. The axial skeleton, which Received 26 August 2013 consists of serially repeating segments commonly known as vertebrae, protects and provides leverage Received in revised form 7 October 2013 for movement of the body. Across the vertebral column, much numerical and morphological diversity Accepted 9 October 2013 can be observed, which is associated with axial regionalization. The present article discusses this basic Available online 5 December 2013 diversity and the early developmental mechanisms that guide vertebral formation and regionalization. An examination of vertebral numbers across the major vertebrate clades finds that actinopterygian and Keywords: chondrichthyan fishes tend to increase vertebral number in the caudal region whereas Sarcopterygii Axial skeleton increase the number of vertebrae in the precaudal region, although exceptions to each trend exist. Given Axial regionality Vertebrae the different regions of axial morphospace that are occupied by these groups, differential developmental Vertebral development processes control the axial patterning of actinopterygian and sarcopterygian species. It is possible that, among a variety of factors, the differential selective regimes for aquatic versus terrestrial locomotion have led to the differential use of axial morphospace in vertebrates. © 2013 Elsevier GmbH. All rights reserved. 1. Introduction performance (Tytell et al., 2010). Both vertebral number and shape of the individual vertebrae have been shown to be useful in One of the major defining characteristics of Vertebrata is having understanding the evolution of body shape variation within (Ward a vertebral column that is composed of serially repeating ossi- and Brainerd, 2007; Bergmann and Irschick, 2012) and across fied, cartilaginous, and ligamentous elements that surround the vertebrate groups (Collar et al., 2013). Furthermore, movement spinal cord and notochord (Schultze and Arratia, 1988; Janvier, of individual vertebrae within the vertebral column has provided 1997). These repeating structures are known as vertebrae. Over insight into diverse behavior patterns of vertebrates (Moon, evolutionary history, vertebrae have taken on many functional 1999). Despite these recent studies, the functional implications of roles including protection of the spinal cord and dorsal aorta vertebral variation still need to be explored. as well as providing attachment points for the axial muscula- In the present article, our aim is to provide a brief overview ture. These functional differences correspond to the structural and of the morphological diversity of vertebrae and the early develop- numerical diversity that we observe across the vertebrate axial mental mechanisms that guide vertebral formation. While doing skeleton. so, we discuss differentiation of the axial skeleton and the mech- For centuries, vertebrae were and continue to be a potent anisms underlying regionalization. We also search for broad-scale morphological character for taxonomic and comparative studies. patterns in the axial skeleton by assembling a large data set con- Since the 1800s, studies have pointed out the effects of envi- sisting of vertebral numbers in the precaudal and caudal regions ronmental variation on vertebral characteristics (Jordan, 1891; from diverse members of the major vertebrate clades. Lastly, we Lindsey, 1975; McDowall, 2008 and references therein). However, highlight exciting avenues for future research. only during the last fifty years have vertebrae become the focus of functional biology research. For example, vertebral number has 2. Postcranial axial skeleton and variation in vertebral provided insight into maximum body length and shape in fishes articulation (Lindsey, 1975), which, in turn, has been shown to have functional consequences on important survival traits such as swimming Although often overshadowed by attention given to the skull, the postcranial system, composed of the axial and appendicular skeletons, provides the skull with movement, suspends the body, ଝ and propels the body through different media. In Chordata, the This article is part of a special issue entitled “Axial systems and their actuation: notochord is the primary axial structure. In Agnatha and some new twists on the ancient body of craniates”. ∗ early Actinopterygii, the notochord continues to be the primary Corresponding author. Tel.: +1 516 877 4204. E-mail address: [email protected] (A.B. Ward). axial structure in embryos and adults. It is not until the arrival of 0944-2006/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.zool.2013.10.006 A.B. Ward, R.S. Mehta / Zoology 117 (2014) 70–76 71 the Gnathostomata that the notochord is replaced by a vertebral column with centra in adults. On examining the axial skeleton, the morphological diversity of individual vertebrae is apparent. Vertebrae are composed of multi- ple components: centra, arches, and intervertebral discs (Schultze and Arratia, 1988). Any of these components can contribute to the morphological and functional diversity of the axial skeleton. Verte- brae have also undergone enlargements, reductions, and fusions, which have added to the challenge of tracking development and evolution. The centrum is the main body of the vertebra; it surrounds and replaces or incorporates the notochord. Vertebrae vary in type based on the relationship of the arches to the centrum, the num- ber of elements forming each centrum, and the embryonic origin of the centrum. Based on embryonic origin, centra may be cat- egorized into four different types: chordacentra (when present as mineralized or calcified rings within the notochordal sheath in actinopterygians), arcocentra (when formed by ossification of cartilage extending from the arches around the notochord), auto- centra (when formed independent of the dorsal and ventral arches), or holocentra (when formed by proliferation of cartilage cells around the notochord that then ossify to form amphicoelous cen- tra) (Gadow, 1933; Arratia et al., 2001). Multiple centra articulate to form the axial column. The artic- ulating surfaces of the centra vary and this variation can affect the movement and the roles of the axial skeleton. Centra with flat ends are termed acoelous whereas centra with concave ends are amphicoelous. Acoelous centra are found in precaudal verte- brae, i.e., mainly the trunk, of early reptiles, birds, and mammals. Amphicoelous centra are found in Chondrichthyes, Actinoptery- gii, and some amphibians, such as the salamander Necturus. Centra that are concave anteriorly and convex posteriorly are called pro- coelous while the reverse of this design is known as opisthocoelous. In the procoelous and opisthocoelous conditions, the centra artic- ulate like a ball-and-socket joint and rotation is at the center of Fig. 1. Regionalization of the vertebral column in Vertebrata. While the vertebral the joint, reducing the possibility of vertebral dislocation. Exam- columns of Chondrichthyes and Actinopterygii are divided into a precaudal and ples of vertebrae with procoelus and opisthocoelous centra can be caudal region, all other groups have more than two regions. In amniotes, regional- found in Lissamphibia and early reptiles. Lastly, heterocoelous cen- ization seems to be based upon the presence or absence of ribs or the variation in tra, which are found in the cervical region of birds and turtles, have ribs along the vertebral column. (A) Mammals have the greatest diversity across the axial skeleton with five distinct regions. Also, despite elongation in specific regions, saddle-shaped articular surfaces at both ends (Liem et al., 2001). mammals still maintain 7 cervical vertebrae and 19–20 thoracolumbar vertebrae. Projections known as apophyses may also be found extending Mammalian precaudal elongation is mostly due to elongation of the individual cen- from the centra and vertebral arches. Depending on their size and tra. (B) Sauropsids have four distinct regions with the thoracolumbar region (also location, apophyses can articulate with other bones, such as ribs, known as abdominal or dorsal) having the greatest number of vertebrae. (C) A bony fish skeleton illustrating the simple divisions of the axial skeleton with the precau- or form interlocking processes, known as zygopophyses, between dal and caudal region. Vertebrae in the caudal region are distinguished from those vertebrae. In some elongate terrestrial amniotes where torsion of in the precaudal region by the presence of hemal arches. the body may be extreme, such as snakes, additional zygopophyses, Line drawings are modified from Parker (1900), Ellenberger et al. (1956), and Romer called zygosphenes and zygantra, may be present on the anterior (1966). and posterior margins, respectively, of the neural spine. It was pro- posed that torsion at the vertebral joints was not possible due to the regionalization across vertebrates (Fig. 1). The vertebral column zygosphene–zygantrum articulations (Mosauer, 1932). However, may be divided into
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